Skip to main content

Interaction between Frankia and Actinorhizal Plants

  • Chapter
Plant-Microbe Interactions

Part of the book series: Subcellular Biochemistry ((SCBI,volume 29))

Abstract

A significant part of the nitrogen in living organisms is derived from atmospheric dinitrogen which gets incorporated into organic compounds by biological or chemical nitrogen fixation. Biological nitrogen fixation is an energy-consuming process performed by the enzyme nitrogenase, which is irreversibly denatured by oxygen. Nitrogenase is formed only by prokaryotes, which in some cases fix nitrogen in symbiosis with higher plants. Two groups of bacteria can enter symbioses with higher plants which lead to the formation of special organs, the root nodules, where the bacteria fix nitrogen while being hosted inside plant cells. The product of nitrogen fixation, ammonium, is exported to the plant, while the plant in turn provides its symbiont with energy sources. Azorhizobium, Bradyrhizobium, and Rhizobium enter symbioses with leguminous plants (with one exception, Parasponia from the Ulmaceae family; Trinick, 1979), and actinomycetes of the genus Frankia induce nodules on the roots of a diverse group of dicotyledonous plants, mostly woody shrubs, which are collectively referred to as actinorhizal plants (Benson and Silvester, 1993). While rhizobia are unicellular, Frankia usually grows in hyphal form, but can also form sporangia and, under certain conditions, nitrogen-fixing vesicles (Benson and Silvester, 1993). Vesicles are formed at the ends of hyphae or on short side branches either in the free-living state under nitrogen starvation and aerobic conditions, or in symbiosis. Within the vesicles, nitrogenase is protected from oxygen (Parsons et al., 1987) by the vesicle envelope, which consists of multiple layers of hopanoids, bacterial steroid lipids (Berry et al., 1993). In contrast to Frankia, rhizobia can use N2 as nitrogen source only in symbiosis (with one exception, Azorhizobium caulinodans ORS571; reviewed by de Bruijn, 1989).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aarts, M. G. M., Dirkse, W. B., Stiekema, W. J., and Perdra, A., 1993, Transportation tagging of a male sterility gene in Arabidopsis, Nature 363:715–717.

    Article  PubMed  CAS  Google Scholar 

  • Akkermans, A. D. L., Huss-Danell, K., and Roelofsen, W., 1981, Enzymes of the tricarboxylic acid cycle and the malate-aspartate shuttle in the N2-fixing endophyte of Alnus glutinosa, Physiol. Plant. 53:289–294.

    Article  CAS  Google Scholar 

  • An, C. S., Wills, J. W., Riggsby, W. S., and Mullin, B. C., 1993, Deoxyribonucleic acid base composition of 12 Frankia isolates, Can. J. Bot. 61:2859–2862.

    Article  Google Scholar 

  • Appleby, C. A., 1984, Leghemoglobin and Rhizobium respiration, Annu. Rev. Plant Physiol. 35:443–478.

    Article  CAS  Google Scholar 

  • Baker, D. D., and Mullin, B. C., 1992, Actinorhizal symbiosis, in Biological Nitrogen Fixation (G. Stacey, R. H. Burris, and H. J. Evans, eds.), pp. 259–292, Chapman and Hall, New York.

    Google Scholar 

  • Bauchrowitz, M. A., Barker, D. G., and Truchet, G., 1995, Lectin genes are expressed throughout root nodule development and during nitrogen-fixation in the Rhizobium-Medicago symbiosis, Plant J. 9:31–43.

    Article  Google Scholar 

  • Bauer, W. D., 1981, Infection of legumes by rhizobia, Annu. Rev. Plant Physiol. 32:407–449.

    Article  CAS  Google Scholar 

  • Benson, D. R., and Silvester, W. B., 1993, Biology of Frankia strains, actinomycete symbionts of actinorhizal plants, Microbiol. Rev. 57:293–319.

    PubMed  CAS  Google Scholar 

  • Berg, R. H., and McDowell, L., 1987, Cytochemistry of the wall of infected cells in Casuarina actinorhizae, Can. J. Bot. 66:2038–2047.

    Google Scholar 

  • Berry, A. M., and Sunell, L. A., 1990, The infection process and nodule development, in The Biology of Frankia and Actinorhizal Plants (C. R. Schwintzer and J. D. Tjepkema, eds.), pp. 61–81, Academic Press, San Diego.

    Google Scholar 

  • Berry, A. M., Torrey, J. G., and McCully, M. E., 1983, The fine structure of the root hair wall and surface mucilage in the actinorhizal host Alnus rubra, in Plant Molecular Biology (R. Goldberg, ed.), pp. 319–327, Liss, New York.

    Google Scholar 

  • Berry, A. M., Harriot, O. T., Moreau, R. A., Osman, S. F., Benson, D. R., and Jones, A. D., 1993, Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase, Proc. Natl. Acad. Sci. USA 90:6091–6094.

    Article  PubMed  CAS  Google Scholar 

  • Burgess, D., and Peterson, R. L., 1987a, Development of Alnus japonica root nodules after inoculation with Frankia strain HFPArI3, Can. J. Bot. 65:1647–1657.

    Article  Google Scholar 

  • Burgess, D., and Peterson, R. L., 1987b, Effect of nutrient conditions on root nodule development in Alnus japonica, Can. J. Bot. 65:1658–1670.

    Article  CAS  Google Scholar 

  • Burris, R. H., 1991, Nitrogenases, J. Biol. Chem. 266:9339–9342.

    PubMed  CAS  Google Scholar 

  • Callaham, D., and Torrey, J. G., 1981, The structural basis of infection of root hairs of Trifolium repens by Rhizobium, Can. J. Bot. 59:1647–1664.

    Article  Google Scholar 

  • Callaham, D., Newcomb, W., Torrey, J. G., and Peterson, R. L., 1979, Root hair infection in actinomycete-induced root nodule initiation in Casuarina, Myrica, and Comptonia, Bot. Gaz. (Suppl.) 140:S1–S9.

    Article  Google Scholar 

  • Campos, F., Carsolio, C., Kuin, H., Bisseling, T., Rocha-Sosa, M., and Sánchez, F., 1995, Characterization and gene expression of nodulin Npv30 from common bean, Plant Physiol. 109:363–370.

    Article  PubMed  CAS  Google Scholar 

  • Chandler, M. R., 1978, Some observations on infection of Arachis hypogaea L. by Rhizobium, J. Exp. Bot. 29:749–755.

    Article  Google Scholar 

  • Chandler, M. R., Date, R. A., and Roughley, R. J., 1982, Infection and root nodule development in Stylosanthes species by Rhizobium, J. Exp. Bot. 33:47–57.

    Article  Google Scholar 

  • Conklin, D. S., McMaster, J. A., Culbertson, M. R., and Kung, C., 1992, COT1, a gene involved in cobalt accumulation in Saccharomyces cerevisiae, Mol. Cell Biol. 12:3678–3688.

    PubMed  CAS  Google Scholar 

  • Cooke, R., Raybak, M., Laudié, M., Grellet, F., Delseny, M., Morris, P.-C., Guerrier, D., Giraudat, J., Quigley, F., Clabault, G., Li, Y.-F., Mache, R., Krivitzky, M., Jean-Jacques Gy, I., Kreis, M., Lecharny, A., Parmentier, Y., Marbach, J., Fleck, J., Clément, B., Philipps, G., Hervé, C., Bardet, C. Tremousaygue, D., Lescure, B., Lacomme, C., Roby, D., Jourjon, M.-F., Chabrier, P., Charpenteau, J.-L., Desprez, T., Amselem, J., Chiapello, H., and Höfte, H., 1996, Further progress towards a catalogue of all Arabisopsis genes: Analysis of a set of 5000 non-redundant ESTs, Plant J. 9:101–124.

    Article  PubMed  CAS  Google Scholar 

  • Dart, P. J., 1977, Infection and development of leguminous nodules, in A Treatise on Dinitrogen Fixation, Vol. 3 (R. W. F. Hardy and W. S. Silver, eds.), pp. 367–472, Wiley, New York.

    Google Scholar 

  • De Bruijn, F. J., 1989, The unusual symbiosis between the diayotrophic stem-nodulating bacterium Azorhizobium caulinodans ORS571 and its host, the tropical legume Sesbania rostrata: Plant and bacterial aspects, in Plant-Microbe Interactions. Molecular Genetics and Perspective, Vol. 3 (T. Kosuge and E. W. Nester, eds.), pp. 457–504, McGraw-Hill, New York.

    Google Scholar 

  • De Bruijn, F. J., Rossbach, S., Schneider, M., Messmer, S., Szeto, W. W., Ausubel, F. M., and Schell, J., 1989, Rhizobium meliloti 1021 has three differentially regulated loci involved in glutamine biosynthesis, none of which is essential for symbiotic nitrogen fixation, J. Bacteriol. 171:1673–1682.

    PubMed  Google Scholar 

  • De Maagd, R. A., Rao, A. S., Mulders, I. H. M., Goosen-De Roo, L., van Loosdrecht, M. C. M., Wijfelman, C. A., and Lugtenberg, B. J. J., 1989, Isolation and characterization of mutants of Rhizobium leguminosarum bv. viciae 248 with altered lipopolysaccharides: Possible role of surface charge or hydrophobicity in bacterial release from the infection thread, J. Baceriol. 171:1143–1150.

    Google Scholar 

  • Dénarié, J., and Cullimore, J., 1993, Lipo-oligosaccharide nodulation factors: A new class of signalling molecules mediating recognition and morphogenesis, Cell 74:951–954.

    Article  PubMed  Google Scholar 

  • Dixon, R. O. D., and Wheeler, C. T., 1983, Biochemical, physiological and environmental aspects of symbiotic nitrogen fixation, in Biological Nitrogen Fixation in Forest Ecosystems: Foundations and Application (J. C. Gordon and C. T. Wheeler, eds.), pp. 107–171, Nijhoff/Junk, The Hague.

    Chapter  Google Scholar 

  • Drake, R., John, I., Farrell, A., Cooper, W., Schuch, W., and Grierson, D., 1996, Isolation and analysis of cDNAs encoding tomato cysteine proteases expressed during leaf senescence, Plant Mol. Biol. 30:755–767.

    Article  PubMed  CAS  Google Scholar 

  • Edwards, J. E., Walker, E. L., and Coruzzi, G. M., 1990, Cell-specific expression in transgenic plants reveals nonoverlapping roles for chloroplast and cytosolic glutamine synthetase, Proc. Natl. Acad. Sci. USA 87:3249–3263.

    Google Scholar 

  • Egli, M. A., Larson, R. J., Hruschka, W. R., and Vance, C. P., 1991, Synthesis of nodulins and nodule-enhanced polypeptides by plant gene-controlled ineffective alfalfa nodules, J. Exp. Bot. 42:969–977.

    Article  CAS  Google Scholar 

  • Fleming, A. I., Wittenberg, J. B., Wittenberg, B. A., Dudman, W. F., and Appleby, C. A., 1987, The purification, characterization and ligand-binding kinetics of hemoglobins from root nodules of the non-leguminous Casuarina glauca-Frankia symbiosis, Biochim. Bioiphys. Acta 911:209–220.

    Article  CAS  Google Scholar 

  • Fortin, M. G., Zechelowska, M., and Verma, D. P. S., 1985, Specific targeting of membrane nodulins to the bacteroid-enclosing compartment in soybean nodules, EMBO J. 4:3041–3046.

    PubMed  CAS  Google Scholar 

  • Gan, S., and Amasino, R. M., 1995, Inhibition of leaf senescence by autoregulated production of cytokinin, Science 270:1986–1988.

    Article  PubMed  CAS  Google Scholar 

  • Gherbi, H., Duhoux, E., Franche, C., Pawlowski, K., Berry, A., and Bogusz, D., 1997, Cloning of a full-length symbiotic hemoglobin cDNA and in situ localization of the corresponding mRNA in Casuarina glauca root nodule, Physiol. Plant. 99:608–616.

    Article  CAS  Google Scholar 

  • Glazebrook, J., Ichige, A., and Walker, G. C., 1993, A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development, Genes Dev. 7:1485–1497.

    Article  PubMed  CAS  Google Scholar 

  • Goethals, K., Van den Eede, G., Van Montagu, M., and Holsters, M., 1990, Identification and characterization of a functional nodD gene in Azorhizobium caulinodans ORS571, J. Bacteriol. 172:2658–2666.

    PubMed  CAS  Google Scholar 

  • Goethals, K., Van Montagu, M., and Holsters, M., 1992, Conserved motifs in a divergent nod box of Azorhizobium caulinodans ORS571 reveals a common structure in promoters regulated by LysR-type proteins, Proc. Natl. Acad. Sci. USA 89:1646–1650.

    Article  PubMed  CAS  Google Scholar 

  • Goetting-Minesky, M. P., and Mullin, B. C., 1994, Differential gene expression in an actinorhizal symbiosis: Evidence for a nodule-specific cysteine proteinase, Proc. Natl. Acad. Sci. USA 91:9891–9895.

    Article  PubMed  CAS  Google Scholar 

  • Guan, C., Ribeiro, A., Akkermans, A. D. L., Jing, Y., van Kammen, A., Bisseling, T., and Pawlowski, K., 1996, Nitrogen metabolism in actinorhizal nodules of Alnus glutinosa: Expression of glutamine synthetase and acetylornithine transaminase, Plant Mol. Biol. 32:1177–1184.

    Article  PubMed  CAS  Google Scholar 

  • Guan, C., Akkermans, A. D. L., Bisseling, T., and Pawlowski, K., 1997, ag13 is expressed in Alnus glutinosa nodules in infected cells during endosymbiont degradation and in the nodule pericycle, Physiol. Plant. 99:601–607.

    Article  CAS  Google Scholar 

  • Hanks, J. F., Tolbert, N. E., and Schubert, K. R., 1981, Localization of enzymes of ureide biosynthesis in peroxisomes and microsomes of nodules, Plant Physiol. 68:65–69.

    Article  PubMed  CAS  Google Scholar 

  • Häser, A., Robinson, D. L., Duc, G., and Vance, C. P., 1992, A mutation in Vicia faba results in ineffective nodules with impaired bacteroid differentiation and reduced synthesis of late nod-ulins, J. Exp. Bot. 43:1397–1407.

    Article  Google Scholar 

  • Hauge, B. M., Hanley, S. M., Cartinhour, S., Cherry, J. M., Goodman, H. M., Koornneef, M., Stam, P., Chang, C., Kempin, S., Medrano, L., and Meyrowitz, E. M., 1993, An integrated genetic/RFLP map of the Arabidopsis thaliana genome, Plant J. 3:745–754.

    Article  CAS  Google Scholar 

  • Heidstra, R., Geurts, R., Franssen, H., Spaink, H. P., van Kammen, A., and Bisseling, T., 1994, Root hair deformation activity of nodulation factors and their fate on Vicia sativa, Plant Physiol. 105:787–797.

    PubMed  CAS  Google Scholar 

  • Hensel, L. L., Grbic, V., Baumgarten, D. A., and Bleecker, A. B., 1993, Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis, Plant Cell 5:553–564.

    PubMed  CAS  Google Scholar 

  • Hewitt, E. J., and Bond, G., 1966, The cobalt requirement of non-legume root nodule plants, J. Exp. Bot. 52:480–491.

    Article  Google Scholar 

  • Hirel, B., Perrot-Rechenmann, C., Maudinas, B., and Gadal, P., 1982, Glutamine synthetase in alder (Alnus glutinosa) root nodules. Purification, properties and cytoimmunochemical localization, Physiol. Plant. 55:197–203.

    Article  CAS  Google Scholar 

  • Hirel, B., Miao, G. H., and Verma, D. P. S., 1993, Metabolic and developmental control of glutamine synthetase genes in legumes and non-legume plants, in Control of Plant Gene Expression (D. P. S. Verma, ed.), pp. 443–458, CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Höfte, H., Desprez, T., Amselem, J., Chiapello, H., Caboche, M., Moisan, A., Jourjon, M. F., Charpenteau, J. L., Berthomieu, P., Guerrier, D., Giraudat, J., Quigley, F., Thomas, F., Yu, D. Y., Mache, R., Raynal, M., Cooke, R., Grellet, F., Delseny, M., Partmentier, Y., Marcillac, G., Gigot, C., Fleck, J., Philipps, G., Axelos, M., Bardet, C., Tremousaygue, D., and Lescure, B., 1993, An inventory of 1152 expressed sequence tags obtained by partial sequencing of cDNAs from Arabidopsis thaliana, Plant J. 4:1051–1061.

    Article  PubMed  Google Scholar 

  • Huss-Danell, K., 1990, The physiology of actinorhizal nodules, in The Biology of Frankia and Actinorhizal Plants (C. R. Schwintzer and J. D. Tjepkema, eds.), pp. 129–156, Academic Press, San Diego, California.

    Google Scholar 

  • Huss-Danell, K., and Bergman, B., 1990, Nitrogenase in Frankia from root nodules of Alnus incana (L.) Moench: Immunolocalization of the Fe-and MoFe-proteins during vesicle differentiation, New Phytol. 116:443–455.

    Article  Google Scholar 

  • Iwahori, S., Kair, R., and Nishi, M., 1994, Subcellular localization of calcium ions within cells of the abscission layer of citrus leaf expiants during abscission, J. Jpn. Soc. Hort. Sci. 63:45–50.

    Article  CAS  Google Scholar 

  • Jacobsen-Lyon, K., Jensen, E. Ø., Jørgensen, J.-E., Marcker, K. A., Peacock, W. J., and Dennis, E. S., 1995, Symbiotic and nonsymbiotic hemoglobin genes of Casuarina glauca, Plant Cell 7:213–223.

    PubMed  CAS  Google Scholar 

  • James, E. K., Sprent, J. I., Sutherland, J. M., McInroy, S. G., and Minchin, F. R., 1992, The structure of nitrogen fixing root nodules on the aquatic mimosoid legume Neptunia plena, Ann. Bot. 69:173–180.

    Google Scholar 

  • Kannenberg, E. L., and Brewin, N. J., 1989, Expression of a cell surface antigen from Rhizobium leguminosarum 3841 is regulated by oxygen and pH, J. Bacteriol. 171:4543–4548.

    PubMed  CAS  Google Scholar 

  • Kardailsky, I., Yang, W.-C., Zalensky, A., van Kammen, A., and Bisseling, T., 1993, The pea late nodulin gene PsNOD6 is homologous to the early nodulin genes ENOD3/14 and is expressed after the leghemoglobin genes, Plant Mol. Biol. 23:1029–1037.

    Article  PubMed  CAS  Google Scholar 

  • King, B. J., Layzell, D. B., and Canvin, D. T., 1986, The role of dark carbon dioxide fixation in root nodules of soybean, Plant Physiol. 81:200–205.

    Article  PubMed  CAS  Google Scholar 

  • Kleemann, G., Alskog, G., Berry, A. M., and Huss-Danell, K., 1994, Lipid composition and nitrogenase activity of symbiotic Frankia (Alnus incana) in response to different oxygen concentrations, Protoplasma 183:107–115.

    Article  CAS  Google Scholar 

  • Lalonde, M., 1980, Techniques and observations of the nitrogen fixing Alnus root nodule symbiosis, in Recent Advances in Biological Nitrogen Fixation (N. S. Subba Rao, ed.), pp. 421–434, Oxford and IBH, New Delhi.

    Google Scholar 

  • Lalonde, M., and Knowles, R., 1975, Ultrastructure, composition and biogenesis of the encapsulation material surrounding the endophyte in Alnus crispa var. mollis root nodules, Can. J. Bot. 53:1951–1971.

    Article  Google Scholar 

  • Ledger, S. E., and Gardner, R. C., 1994, Cloning and characterization of five cDNAs for genes differentially expressed during fruit development of kiwifruit (Actinidia deliciosa var. deliciosa), Plant Mol. Biol. 25:877–886.

    Article  PubMed  CAS  Google Scholar 

  • Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Promé, J.-C., and Dénarié, J., 1990, Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal, Nature 344:781–784.

    Article  PubMed  CAS  Google Scholar 

  • Lister, C., and Dean, C., 1993, Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana, Plant J. 4:745–750.

    Article  CAS  Google Scholar 

  • Liu, Q., and Berry, A. M., 1991, The infection process and nodule initiation in the Frankia-Ceanothus root nodule symbiosis: A structural and histochemical study, Protoplasma 163:82–92.

    Article  Google Scholar 

  • Machado, C. R., Costa de Oliveira, R. L., Boiteux, S., Praekelt, U. M., Meacock, P. A., and Menck, C. F. M., 1996, Thil, a thiamine biosynthetic gene in Arabidopsis thaliana, complements bacterial defects in DNA repair, Plant Mol. Biol. 31:585–593.

    Article  PubMed  CAS  Google Scholar 

  • Manen, J. F., Simon, P., van Slooten, J.-C., ØsterÃ¥s, M., Frutiger, S., and Hughes, G. J., 1991, A nodulin specifically expressed in senescent nodules of winged bean is a protease inhibitor, Plant Cell 3:259–270.

    PubMed  CAS  Google Scholar 

  • Martin, T., Frommer, W. B., Salanoubat, M., and Willmitzer, L., 1993, Expression of an Arabidopsis sucrose synthase gene indicates a role in metabolization of sucrose both during phloem loading and in sink organs, Plant J. 4:367–377.

    Article  PubMed  CAS  Google Scholar 

  • McClure, P. R., Coker, G. T., and Schubert, K. R., 1983, Carbon dioxide fixation in roots and nodules of Alnus glutinosa. I. Role of phosphoenolpyruvate carboxylase and carbamyl phosphate synthetase in dark CO2 fixation, citrulline synthesis, and N2 fixation, Plant Physiol. 71:652–657.

    Article  PubMed  CAS  Google Scholar 

  • Meyen, J., 1829, Ãœber das Hervorwachsen parasitischer Gebilde aus den Wurzeln anderer Pflanzen, Flora 12:49–64.

    Google Scholar 

  • Miao, G.-H., Hirel, B., Marsolier, M. C., Ridge, R. W., and Verma, D. P. S., 1991, Ammonia-regulated expression of a soybean gene encoding cytosolic glutamine synthetase in transgenic Lotus corniculatus, Plant Cell 3:11–22.

    PubMed  CAS  Google Scholar 

  • Miller, I. M., and Baker, D. D., 1985, The initiation, development and structure of root nodules in Elaeagnus angustifolia L. (Elaeagnaceae), Protoplasma 128:107–119.

    Article  Google Scholar 

  • Morell, M., and Copeland, L., 1984, Enzymes of sucrose breakdown in soybean nodules. Alkaline invertase, Plant Physiol. 74:1030–1034.

    Article  PubMed  CAS  Google Scholar 

  • Morell, M., and Copeland, L., 1985, Sucrose synthase of soybean nodules, Plant Physiol. 78:149–154.

    Article  PubMed  CAS  Google Scholar 

  • Mullin, B. C., Goetting-Minesky, P., and Twigg, P., 1993, Differential gene expression in the development of actinorhizal root nodules, in: New Horizons in Nitrogen Fixation (R. Palacios, J. Mora, and W. E. Newton, eds.), pp. 309–314, Kluwer, Dordrecht, The Netherlands.

    Chapter  Google Scholar 

  • Mylona, P., Pawlowski, K., and Bisseling, T., 1995, Symbiotic nitrogen fixation, Plant Cell 7:869–885.

    PubMed  CAS  Google Scholar 

  • Nap, J. P., and Bisseling, T., 1990, Developmental biology of a plant-prokaryote symbiosis: The legume root nodule, Science 250:948–954.

    Article  PubMed  CAS  Google Scholar 

  • Newcomb, W., 1976, A correlated light and electron microscopic study of symbiotic growth and differentiation in Pisum sativum rootnodules, Can. J. Bot. 54:2163–2186.

    Article  Google Scholar 

  • Newcomb, W., and Wood, S. M, 1987, Morphogenesis and fine structure of Frankia (Actinomycetales): The microsymbiont of nitrogen-fixing actinorhizal root nodules, Int. Rev. Cytol. 109:1–88.

    Article  PubMed  CAS  Google Scholar 

  • Newcomb, W., Sippel, D., and Peterson, R. L., 1979, The early morphogenesis of Glycine max and Pisum sativum root nodules, Can. J. Bot. 57:2603–2616.

    Article  Google Scholar 

  • Newman, T., de Bruijn, F. J., Green, P., Keegstra, K., Kende, H., McIntosh, L., Ohlrogge, J., Raikhel, N., Somerville, S., Thomashow, M., Retzel, E., and Somerville, C., 1994, Genes galore: A summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones, Plant Physiol. 106:1241–1255.

    Article  PubMed  CAS  Google Scholar 

  • Nguyen, T., Zelechowska, M., Forster, V., Bergmann, H., and Verma, D. P. S., 1985, Primary structure of the soybean nodulin-35 gene encoding uricase II localized in the peroxisomes of uninfected cells of nodules, Proc. Natl. Acad. Sci. USA 82:5040–5044.

    Article  PubMed  CAS  Google Scholar 

  • Oliver, S. G., 1996, From DNA sequence to biological function, Nature 379:597–600.

    Article  PubMed  CAS  Google Scholar 

  • Ouyang, L.-J., Whelan, J., Weaver, C. D., Roberts, D. M., and Day, D. A., 1991, Protein phosphorylation stimulates the rate of malate uptake across the peribacteroid membrane of soybean nodules, FEBS Lett. 293:188–190.

    Article  PubMed  CAS  Google Scholar 

  • Parsons, R., Silvester, W. B., Harris, S., Gruijters, W. T. M., and Bullivant, S., 1987, Frankia vesicles provide inducible and absolute oxygen protection for nitrogenase, Plant Physiol. 83:728–731.

    Article  PubMed  CAS  Google Scholar 

  • Pate, J. S., 1962, Root exudation studies on the exchange of 14C-labeled organic substances between the roots and shoot of the nodulated legumes, Plant Soil 17:333–356.

    Article  CAS  Google Scholar 

  • Pawlowski, K., Guan, C., Ribeiro, A., van Kammen, A., Akkermans, A. D. L., and Bisseling, T., 1994a, Genes involved in Alnus glutinosa nodule development, in Proceedings of the 1st European Nitrogen Fixation Conference (G. B. Kiss and G. Endre, eds.), pp. 220–224. Officina Press, Szeged, Hungary.

    Google Scholar 

  • Pawlowski, K., Ribeiro, A., Guan, C., van Kammen, A., Akkermans, A. D. L., and Bisseling, T., 1994b, Differential gene expression in root nodules of Alnus glutinosa, in Nitrogen Fixation with Non-Legumes (N. A. Hegazi, M. Fayez, and M. Monib, eds.), pp. 185–190, The American University in Cairo Press, Cairo.

    Google Scholar 

  • Pawlowski, K., Akkermans, A. D. L., van Kammen, A., and Bisseling, T., 1995, Expression of Frankia nif genes in nodules of Alnus glutinosa, Plant Soil 170:371–376.

    Article  CAS  Google Scholar 

  • Pawlowski, K., Twigg, P., Dobritsa, S., Guan, C., and Mullin, B. C., 1997, A nodule-specific gene family from Alnus glutinosa encodes glycine-and histidine-rich proteins expressed in the early stages of actinorhizal nodule development, Mol. Plant-Microbe Interact. 10:656–664.

    Article  PubMed  CAS  Google Scholar 

  • Perotto, S., Donovan, N., Drobak, B. K., and Brewin, N. J., 1995, Differential expression of a glycosyl inositol phospholipid antigen on the peribacteroid membrane during pea nodule development, Mol. Plant-Microbe Interact. 8:560–568.

    Article  CAS  Google Scholar 

  • Peterman, T. K., and Goodman, H. M., 1991, The glutamine synthetase gene family of Arabidopsis thaliana: Light-regulation and differential expression in leaves, roots and seeds, Mol. Gen. Genet. 230:145–154.

    Article  PubMed  CAS  Google Scholar 

  • Pfeiffer, N. E., Malik, N. S. A., and Wagner, F. W., 1983a, Reversible dark-induced senescence of soybean root nodules, Plant Physiol. 71:393–399.

    Article  PubMed  CAS  Google Scholar 

  • Pfeiffer, N. E., Malik, N. S. A., and Wagner, F. W., 1983b, Proteolytic activity in soybean root nodules, Plant Physiol. 71:797–802.

    Article  PubMed  CAS  Google Scholar 

  • Pladys, D., and Vance, C. P., 1993, Proteolysis during development and senescence of effective and plant gene-controlled ineffective alfalfa nodules, Plant Physiol. 103:379–384.

    PubMed  CAS  Google Scholar 

  • Pladys, D., Dimitrijevic, L., and Rigaud, J., 1991, Localization of a protease in protoplast preparations in infected cells of French bean nodules, Plant Physiol. 97:1174–1180.

    Article  PubMed  CAS  Google Scholar 

  • Praekelt, U. M., and Meacock, P. A., 1992, MOL1, a Saccharomyces cerevisiae gene that is highly expressed in early stationary phase during growth on molasses, Yeast 8:699–710.

    Article  PubMed  CAS  Google Scholar 

  • Praekelt, U. M., Byrne, K. L., and Meacock, P. A., 1994, Regulation of THI4 (MOL1), a thiamine-biosynthetic gene of Saccharomyces cerevisiae, Yeast 10:481–490.

    Article  PubMed  CAS  Google Scholar 

  • Racette, S., and Torrey, J. G., 1989, Root nodule initiation in Gymnostoma (Casuarinaceae) and Shepherdia (Elaeagnaceae) induced by Frankia strain HFPGpI1, Can. J. Bot. 67:2873–2879.

    Article  Google Scholar 

  • Reddy, A., Bochenek, B., and Hirsch, A. M., 1992, A new Rhizobium meliloti symbiotic mutant isolated after introducing Frankia DNA sequence into a nodA:Tn5 strain, Mol. Plant-Microbe Interact. 5:62–71.

    Article  CAS  Google Scholar 

  • Ribeiro, A., Akkermans, A. D. L., van Kammen, A., Bisseling, T., and Pawlowski, K., 1995, A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development, Plant Cell 7:785–794.

    PubMed  CAS  Google Scholar 

  • Ribeiro, A., Praekelt, U., Akkermans, A. D. L., Meacock, P., van Kammen, A., Bisseling, T., and Pawlowski, K., 1996, Identification of agthi1, encoding an enzyme involved in biosynthesis of the thiamine precursor thiazole, in actinorhizal nodules of Alnus glutinosa, Plant J. 10:361–368.

    Article  PubMed  CAS  Google Scholar 

  • Roberts, M. P., Jafar, S., and Mullin, B. C., 1985, Leghemoglobin-like sequences in the DNA of four actinorhizal plants, Plant Mol. Biol. 5:333–337.

    Article  CAS  Google Scholar 

  • Roche, D., Temple, S. J., and Sengupta-Gopalan, C., 1993, Two classes of differentially regulated glutamine synthetase genes are expressed in the soybean nodule: A nodule-specific class and a constitutively expressed class, Plant Mol. Biol. 22:971–983.

    Article  PubMed  CAS  Google Scholar 

  • Ronson, C. W., Astwood, P. M., Nixon, B. T., and Ausubel, F. M., 1987, Deduced products of C4-dicarboxylate transport regulatory genes of Rhizobium leguminosarum are homologous to nitrogen regulatory gene products, Nucleic Acids Res. 15:7921–7935.

    Article  PubMed  CAS  Google Scholar 

  • Sanchez, F., Padilla, J. E., Perez, H., and Lara, M., 1991, Control of nodulin genes in root-nodule development and metabolism, Annu. Rev. Plant Physiol. Plant Mol. Biol. 42:507–528.

    Article  CAS  Google Scholar 

  • Sandal, N. N., Bojsen, K., and Marcker, K. A., 1987, A small family of nodule specific genes from soybean, Nucleic Acids Res. 15:1507–1519.

    Article  PubMed  CAS  Google Scholar 

  • Schlaman, H. R. W., Horvath, B., Vijgenboom, E., Okker, R. J. H., and Lugtenberg, B. J. J., 1991, Evidence for a new negative regulation mechanism involved in the suppression of nodulation gene expression of Rhizobium leguminosarum bv. viciae, J. Bacteriol. 173:4277–4287.

    PubMed  CAS  Google Scholar 

  • Schubert, K. R., 1986, Products of biological nitrogen fixation in higher plants: Synthesis, transport, and metabolism, Annu. Rev. Plant Physiol. 37:539–574.

    Article  CAS  Google Scholar 

  • Schwintzer, C. R., Berry, A. M., and Disney, L. D., 1982, Seasonal patterns of root nodule growth, endophyte morphology, nitrogenase activity and shoot development in Myrica gale, Can. J. Bot. 60:746–757.

    Article  Google Scholar 

  • Séguin, A., and Lalonde, M., 1990, Micropropagation, tissue culture, and genetic transformation of actinorhizal plants and Betula, in The Biology of Frankia and Actinorhizal Plants (C. R. Schwintzer and J. D. Tjepkema, eds.), pp. 215–238, Academic Press, San Diego, California.

    Google Scholar 

  • Séguin, A., and Lalonde, M., 1993, Modification of polypeptide patterns during nodule development in the Frankia-Alnus symbiosis, Symbiosis 15:135–149.

    Google Scholar 

  • Selker, J. M. L., 1988, Three-dimensional organization of uninfected tissue in soybean root nodules and its relation to cell specialization in the central region, Protoplasma 147:178–190.

    Article  Google Scholar 

  • Sellstedt, A., and Atkins, C. A., 1991, Composition of amino compounds transported in xylem of Casuarina sp., J. Exp. Bot. 42:1493–1497.

    Article  CAS  Google Scholar 

  • Silvester, W. B., and Harris, S. L., 1989, Nodule structure and nitrogenase activity of Coriaria arborea in response to varying pO2, Plant Soil 118:97–109.

    Article  CAS  Google Scholar 

  • Silvester, W. B., Harris, S. L., and Tjepkema, J. D., 1990, Oxygen regulation and hemoglobin, in The Biology of Frankia and Actinorhizal Plants (C. R. Schwintzer and J. D. Tjepkema, eds.), pp. 157–176, Academic Press, San Diego, California.

    Google Scholar 

  • Simonet, P., Normand, P., Hirsch, A. M., and Akkermans, A. D. L., 1990, The genetics of the Frankia-actinorhizal symbiosis, in Molecular Biology of Symbiotic Nitrogen Fixation (P. M. Gresshoff, ed.), pp. 77–109, CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Smart, C. M., 1994, Gene expression during leaf senescence, New Phytol. 126:419–448.

    Article  CAS  Google Scholar 

  • Soltis, D. E., Soltis, P. S., Morgan, D. R., Swensen, S. M., Mullin, B. C., Dowd, J. M., and Martin, P. G., 1995, Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms, Proc. Natl. Acad. Sci. USA 92:2647–2651.

    Article  PubMed  CAS  Google Scholar 

  • Soupène, E., Foussard, M., Boistard, P., Truchet, G., and Batut, J., 1995, Oxygen as a key developmental regulator of Rhizobium meliloti N2-fixation gene expression within the alfalfa root nodule, Proc. Natl. Acad. Sci. USA 92:3759–3763.

    Article  PubMed  Google Scholar 

  • Sprent, J. I., 1989, Which steps are essential for the formation of functional legume nodules? New Phytol. 111:129–153.

    Article  Google Scholar 

  • Thummler, F., and Verma, D. P. S., 1987, Nodulin-100 of soybean is the subunit of sucrose synthase regulated by the availability of free heme in nodules, J. Biol. Chem. 262:14730–14736.

    PubMed  CAS  Google Scholar 

  • Tjepkema, J. D., 1983, Oxygen concentration within the nitrogen-fixing root nodules of Myrica gale L., Am. J. Bot. 70:59–63.

    Article  Google Scholar 

  • Tjepkema, J. D., and Asa, D. J., 1987, Total and CO-reactive heme content of actinorhizal nodules and the roots of some non-nodulated plants, Plant Soil 100:225–236.

    Article  CAS  Google Scholar 

  • Torrey, J. G., and Callaham, D., 1978, Determinate development of nodule roots in actinomycete-induced root nodules of Myrica gale, Can. J. Bot. 56:1357–1364.

    Article  Google Scholar 

  • Tremblay, F. M., Pérmet, P., and Lalonde, M., 1986, Tissue culture of Alnus spp. with regard to symbioses, in Biotechnology in Agriculture and Forestry (Y. P. S. Bajaj, ed.), pp. 87–100, Springer-Verlag, Berllin.

    Google Scholar 

  • Trinick, M. J., 1979, Structure of nitrogen-fixing nodules formed by Rhizobium on roots of Parasponia andersonii, Appl. Environ. Microbiol. 55:2046–2055.

    Google Scholar 

  • Tsay, Y. F., Schroeder, J. I., Feldmann, K. A., and Crawford, N. M., 1993, The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter, Cell 72:705–713.

    Article  PubMed  CAS  Google Scholar 

  • Valpuesta, V., Lange, N. E., Guerrero, C., and Reid, M. S., 1995, Up-regulation of a cysteine protease accompanies the ethylene-insensitive senescence of daylily (Hemerocallis) flowers, Plant Mol. Biol. 28:575–582.

    Article  PubMed  CAS  Google Scholar 

  • Vance, C. P., and Heichel, G. H., 1991, Carbon in N2-fixation: Limitation or exquisite adaption, Annu. Rev. Plant Physiol. Plant Mol. Biol. 42:373–392.

    Article  CAS  Google Scholar 

  • Van der Straeten, D., Rodrigues-Pousada, R. A., Goodman, H. M., and Van Montagu, M., 1991, Plant enolase: Gene structure, expression, and evolution, Plant Cell 3:719–735.

    PubMed  Google Scholar 

  • Van de Wiel, C., Scheres, B., Franssen, H., van Lierop, M. J., van Lammeren, A., van Kammen, A., and Bisseling, T., 1990, The early nodulin transcript ENOD2 is located in the nodule parenchyma (inner cortex) of pea and soybean root nodules, EMBO J. 9:1–7.

    PubMed  Google Scholar 

  • Van Ghelue, M., Ribeiro, A., Solheim, B., Akkermans, A. D. L., Bisseling, T., and Pawlowski, K., 1996, Sucrose synthase and enolase expression in actinorhizal nodules of Alnus glutinosa: Comparison with legume nodules, Mol. Gen. Genet. 250:437–446.

    Article  PubMed  Google Scholar 

  • Van Ghelue, M., Løvaas, E., Ringø, E., and Solheim, B., 1997, Early interactions between Alnus glutinosa (L.) Gaertn. and Frankia strain ArI3, Physiol. Plant. 99:579–587.

    Article  Google Scholar 

  • Van Kammen, A., 1984, Suggested nomenclature for plant genes involved in nodulation and symbiosis, Plant Mol. Biol. Rep. 2:43–45.

    Article  Google Scholar 

  • Van Rhijn, P., and Vanderleyden, J., 1995, The Rhizobium-plant symbiosis, Microbiol. Rev. 59:124–142.

    PubMed  Google Scholar 

  • Vasse, J., de Billy, F., Camut, S., and Truchet, G., 1990, Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules, J. Bacteriol. 172:4295–4306.

    PubMed  CAS  Google Scholar 

  • Vercher, Y., and Carbonell, J., 1991, Changes in the structure of ovary tissues and in the ultrastructure of mesocarp cells during ovary senescence or fruit development induced by plant growth substances in Pisum sativum, Physiol. Plant 81:518–526.

    Article  CAS  Google Scholar 

  • Verma, D. P. S., 1992, Signals in root nodule organogenesis and endocytosis of Rhizobium, Plant Cell 4:373–382.

    PubMed  CAS  Google Scholar 

  • Weaver, C. D., Shower, N. H., Louis, C. F., and Roberts, D. M., 1994, Nodulin-26, a nodule specific symbiosome membrane protein from soybean, is an ion channel, J. Biol. Chem. 269:17858–17862.

    PubMed  CAS  Google Scholar 

  • Werner, D., 1992, Physiology of nitrogen-fixing legume nodules: Compartments and functions, in Biological Nitrogen Fixation (G. Stacey, R. H. Burris, and H. J. Evans, eds.), pp. 399–431, Chapman & Hall, New York.

    Google Scholar 

  • Witty, J. F., Minchin, F. R., Skøt, L., and Sheely, J. E., 1986, Nitrogen fixation and oxygen in root nodules, Oxford Surv. Plant Cell Biol. 3:275–315.

    CAS  Google Scholar 

  • Yang, W.-C., Horvath, B., Hontelez, J., van Kammen, A., and Bisseling, T., 1991, In situ localization of Rhizobium mRNAs in pea root nodules: nifA and nifH localization, Mol. Plant-Microbe Interact. 4:464–468.

    Article  Google Scholar 

  • Zeng, S., and Tjepkema, J. D., 1994, The wall of the infected cell may be the major diffusion barrier in nodules of Myrica gale L., Soil Biol. Biochem. 5:633–639.

    Article  Google Scholar 

  • Zeng, S., Tjepkema, J. D., and Berg, R. H., 1989, Gas diffusion pathway in nodules of Casuarina cunninghamiana, Plant Soil 118:119–123.

    Article  Google Scholar 

  • Zhang, Y., and Roberts, D. M., 1995, Expression of soybean nodulin 26 in transgenic tobacco. Targeting to the vacuolar membrane and effects on floral and seed development, Mol. Biol. Cell 6:109–117.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1998 Springer Science+Business Media New York

About this chapter

Cite this chapter

Guan, C., Pawlowski, K., Bisseling, T. (1998). Interaction between Frankia and Actinorhizal Plants. In: Biswas, B.B., Das, H.K. (eds) Plant-Microbe Interactions. Subcellular Biochemistry, vol 29. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-1707-2_5

Download citation

  • DOI: https://doi.org/10.1007/978-1-4899-1707-2_5

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4899-1709-6

  • Online ISBN: 978-1-4899-1707-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics